Ultrasonographic Characteristics in the Fingers and Other Superficial Glomus Tumours

Glomus tumours are painful superficial tumours, and ultrasonography is an extremely useful and noninvasive diagnostic technique for superficial organs. In this study, we retrospectively examined glomus tumours using ultrasonography. Among 18 patients histopathologically diagnosed with glomus tumours via ultrasonography, we observed five different development sites: subungual areas or those surrounding the nail bed (12), other areas on the finger surface (3), abdominal wall (1), upper arm (1), and forearm (1). The ultrasonographic images revealed significant differences in tumour size, indicating that tumours on other body surfaces tended to be smaller than those on patients' fingers (p < 0.01). The depth/width ratios of tumours on the other body surfaces were significantly higher than those on the fingers (p < 0.05). The tumours showed a regular shape (72.2%) and clear border (100%). Furthermore, most tumours were low-echo tumours with a diameter of up to 15 mm, clear margins, and no lateral shadows. Abundant blood flow and vessels in and out of the tumours were also observed. In conclusion, our study describes the ultrasonographic characteristics of glomus tumours and reveals that they cannot be ruled out when diagnosing small painful subcutaneous tumours.


Introduction
Glomus tumours were frst described by Masson, who observed a specialised form of arteriovenous anastomosis in the peripheral areas of the skin and described it as a glomus neuromyoartrial formation, in 1924 [1]. As the histological images were similar to those of tumours, these nodules were originally described as glomus tumours or arterial angioneuromyoma [1]. Glomus tumours are relatively rare, benign, vascular tumours that can either be classifed as solitary or multiple tumours (with the former accounting for the majority of cases) [2][3][4]. Solitary glomus tumours frequently develop in subungual areas and are accompanied by spontaneous pain, which tends to intensify with compression, cold, and other factors [5,6]. Indeed, glomus tumours should be primarily suspected when a painful subungual tumour is observed. However, tumours that grow on body surfaces other than subungual areas must frst be diferentiated from other types of superfcial, painful tumours rather than directly classifed as glomus tumours [7][8][9][10]. Such diagnoses are typically performed through histopathological examination by biopsy; therefore, the ultrasonographic characteristics of such tumours remain unclear [6]. Nevertheless, ultrasonography is an extremely useful and noninvasive diagnostic aid for superfcial organs such as the lymph nodes, breasts, and lips [11][12][13][14]. Hence, in this study, we retrospectively examine the ultrasonographic characteristics of glomus tumours, including those found on nonsubungual body surfaces.

Materials and Methods
2.1. Subjects. All patients provided verbal and written informed consent to participate in this study. Furthermore, the study was approved by the review board of Tokai University (18R192). Te subjects included 18 patients (four men and fourteen women; mean age, 54 (range, 23-82) years) who were histopathologically diagnosed with glomus tumours following ultrasonography on painful superfcial tumours in Tokai University Hospital from April 2012 to December 2018. Tis study only involved patients with solitary tumours. Te following ultrasonography devices were used on the subjects: TUS-A300, TUS-A500, and SSA-790A (Canon Medical Systems Corporation). Te following probes were employed, all with a frequency range of 5-18 MHz: PLT-1204BX, PLT-1204BT, and PLT-1204BX.

Study
Procedure. Te following tumour-related features were retrospectively examined with reference to ultrasonographic images: sites of development, maximum diameter, depth/width ratio, shape, border, lateral shadow, internal echo, posterior echo, blood fow, and high echo surrounding the tumour. Tumour shapes were either round, squamous, or elliptical, whereas tumours with corners and constrictions were considered to be irregular. Tumours with a depth/width ratio of less than 0.5 were deemed to be squamous in shape. A clear border refers to the boundary between the tumour and the surrounding tissue; if the tumour and surrounding tissue could not be distinguished, the border was considered unclear, with a sectional border being partially unclear. Lateral shadows could occur on both or one side of the tumour. Blood fow was evaluated using colour Doppler or power Doppler methods. Tumours were categorised according to the proportion of a single image attributed to blood fow, i.e., a high blood-fow pattern indicated that blood fow was observed throughout the tumour; a low blood-fow pattern indicated that blood fow was observed in up to 50% of the total tumour area; and a moderate blood-fow pattern indicated blood fow between these two extremes. Moreover, for fve patients who were subjected to blood-fow velocity measurement using the pulse Doppler method, we examined the presence of blood vessels fowing in and out of the tumour and measured the maximum blood fow velocity. Ultrasonographic images were evaluated by a registered medical sonographer for superfcial regions certifed by the Japan Society of Ultrasonics in Medicine with >10 years of experience. Welch's t-test was used to test for signifcance, and the statistical signifcance was set to p < 0.05 or p < 0.01.

Developmental Sites.
Twelve patients had glomus tumours in subungual regions or areas surrounding the nail bed (67%), which accounted for the most common developmental site. Te remaining six glomus tumours occurred on the fnger surface (specifcally on the thumb) in three patients (17%), the abdominal wall in one patient (6%), the upper arm in one patient (6%), and the forearm in one patient (6%). Tus, glomus tumours developed on the fngers in 15 out of 18 patients (83%).

Tumour Size and Depth/Width
Ratio. Te mean maximum diameter was 6.8 mm (3-15 mm). Tumour diameters of ≥10 mm, 5-10 mm, and <5 mm were observed in four patients (22.2%), seven patients (38.9%), and seven patients (38.9%), respectively. Tumours <10 mm accounted for 77.8% of all tumours. No tumours ≥10 mm were observed on body parts other than the fngers. According to ultrasonographic analysis, the maximum tumour diameter in the 15 patients with tumours of the fnger was 3-15 mm (mean, 7.3 mm), whereas that in the other three patients was 4-5 mm (mean, 4.3 mm). Welch's t-test showed a signifcant diference in the maximum diameter between tumours on the fngers and those on other parts of the body (p < 0.01) ( Table 1).
Te mean depth/width ratio for all patients was 0.58 (0.29-1.0). For the ffteen patients with tumours of the fnger, the mean depth/width ratio was 0.53. For the three patients with tumours on other body surfaces, the mean depth/width ratio was 0.83 (Table 1). Te depth/width ratios of tumours on the other body surfaces were signifcantly higher than those on the fngers (p < 0.05). We then compared the six tumours on patients' fngers that were ≦5 mm with the three tumours on other body surfaces and observed that the mean maximum diameters were 0.65 and 0.83, respectively, However, no signifcant diference was observed between the two groups (p = 0.13) ( Table 2).

Shape
Te tumour shape was regular in 13 patients (72%) and irregular in fve patients (28%). Among the regular tumour shapes, fve were elliptical, six were squamous, and two were round ( Figure 1). Clear and partially unclear borders were observed in seventeen patients (94%) and one patient (6%), respectively. Most of the fnger masses were elliptical or squamous: elliptical in seven patients, round in one patient, squamous in four patients, and irregular in three patients. Other glomus tumours on the body surface were small spherical or irregularly shaped masses with a higher depth/ width ratio.

Internal and Posterior Echo.
Te internal echo of solid hypoechoic tumour was even in fourteen patients (78%) and uneven in four patients (22%). Fine echogenic spots were observed internally in three patients ( Figure 2). No tumours were accompanied by cystic portions internally. Posterior echo was enhanced in fourteen patients (78%) and unchanged in four patients (22%). None of the tumours were attenuated. Moreover, the degree of enhancement was small in seven of the fourteen patients with enhanced posterior echo.

Blood-Flow Evaluation.
Te blood-fow patterns observed by power or colour Doppler ultrasound were high in six patients (33%), moderate in eleven patients (61%), and low in one patient (6%) (Figure 3). In addition, vessels fowing in and out of the tumour were observed in fourteen patients (78%) (Figure 4). Te maximum blood fow velocity in fve patients whose blood infow and outfow was measured via the pulse Doppler method was 5.0-13.8 cm/s (mean, 7.7 cm/s) ( Table 3).

High Echo Surrounding the Tumour.
High echo surrounding the tumour was observed in two patients (11%). Tis high echo was observed in the subcutaneous fat of    tumours that grew on body surfaces other than the fngers. For example, in the glomus tumour that developed on the abdominal wall, high echo with unclear margins around the tumour was observed in the subcutaneous fat layer ( Figure 5). Histopathological examination revealed a nodule with clear margins within the adipose tissue, and densely packed cubic tumour cells enlarged to an oval shape proliferated in a cobblestone-like pattern (top left). In enlarged magnifcation, small difuse vessels were observed within the adipose tissue of areas surrounding the nodule (lower left).

Discussion
In this study, we retrospectively analysed ultrasonographic images of glomus tumours located in subungual or other areas in 18 patients. Te most frequent sites of development were the subungual regions and areas surrounding the nail bed. Tumours on the fngers, including the thumb, were noted in 83% of patients in this study. Glomus tumours are painful tumours that frequently grow subungually but can also grow on other areas of the body. A previous analysis of tumour development sites in 126 patients reported the following proportions: 66% on the hand, 11% on the forearm, 9% on the thigh, 5% on the upper arm, 3% on the lower leg, 2% on the foot, 2% on the head and neck, and 1% on the trunk [15]. Tese results suggest that glomus tumours do not only refer to painful solid tumours on the fngers. Our study confrmed these previous fndings, that is, glomus tumours were observed in areas other than the fngers in three patients (i.e., abdominal wall, upper arm, and forearm). However, a diferential diagnosis by ultrasonography for these three patients may not typically include glomus tumours. Tus, despite their low incidence, it is necessary to also consider glomus tumours in the diferential diagnosis of painful subcutaneous tumours that grow in areas other than the fngers. Te ultrasonographic images revealed signifcant differences in the mean maximum diameter of tumours, indicating that tumours on other body surfaces of patients tended to be smaller than those on their fngers (p < 0.01). Te ultrasonographic images revealed signifcant diferences in tumour mean depth/width ratio, indicating that the tumours on patients' fngers tended to be smaller than those on other body surfaces (p < 0.05). Tese results suggest that fnger glomus tumours tend to be elliptical or rather fat, whereas tumours on other body surface tend to have a high depth/width ratio.
A lateral shadow was observed in only two patients (88%). A lateral shadow is an image artifact wherein the lateral posterior side of the tumour is missing; this occurs when the speed of sound inside the tumour is slower than that in the surrounding tissue. In this case, the sound wave which travels into the tumour is refracted and converges inward, whereas the rest of the sound wave is refected upon impact at the critical angle in areas near the boundary of the spherical tumour, thereby leading to a decrease in the transmitted wave in these areas. Ultrasonic wave refraction is greater in cysts and round-shaped tumours and tends to cause lateral shadows. In tumours with irregular borders, a lateral shadow is unlikely because the ultrasonic waves are scattered. Although the tumours examined in this study were not fully compared with pathological tissue samples, fbrous capsules, including partial fbrous capsules, were observed in 15 of 16 patients (assessment could not be performed in two of the patients). Most of these fbrous capsules were thin ( Figure 6); a relatively thick and even fbrous capsule was observed in one patient only, who had a small tumour with a maximum diameter of 3 mm. Te two tumours with lateral shadows were covered by a fbrous    capsule, which had diameters of 15 mm and 4 mm. Te lack of lateral shadows was attributed to the small diference in the speed of sound between the tissue surrounding the tumour and that inside the tumour and the limited impact of the critical angle generally caused by a small tumour size. Solid tumours were observed in fourteen patients (78%) with an even internal echo. Uneven internal echo was observed in four patients, of which three had a tumour with fne echo spots or hyperechoic strands internally. No tumours had an acoustic shadow, which may be because relatively thick vessel walls and collagen fbres were drawn in the form of high-echo intensity caused by posterior scattering. Enhanced posterior echo was observed in fourteen patients (78%); this was attributed to the increased permeability caused by a limited decrease in ultrasonic waves from a decrease in the diference in acoustic impedance, which refects the proliferation of sheet-and cord-like tumour cells and mucus-like substrates.
Blood-fow patterns inside the tumours were evaluated using colour Doppler or power Doppler methods. A moderate blood-fow pattern, which indicated the presence of blood fow in at least 50% of the tumour, was observed in 17 patients (94%). Tus, abundant blood-fow signals were observed in all tumours. Fan et al. studied 62 patients and showed abundant blood-fow signals in 38.7% (24/62) of tumours, low blood-fow signals in 35.5% (22/62) of tumours, and no blood-fow signals in 19.4% (16/62) of tumours. Te absence of blood-fow signals occurred in tumours with few blood vessels, i.e., glomangiomyoma or myxoid glomus tumours, wherein dilated vessels were accompanied by thrombus [16]. In our study, none of the 18 patients had glomangiomyomas. Moreover, blood-fow signals tend to be low in the glomus and myxoid tumour subtypes; thus, pain is a typical clinical symptom in these tumour types. However, histological changes may occur in    [16]. However, previous studies did not provide mean or median values. In the fve patients examined in this study, pulsation waves were noted in the tumours, with a maximum velocity of 15 cm/s considered as an indicator of glomus tumours. High echo around the tumours were observed in only two patients, who had tumours on body surfaces other than the fngers, specifcally, on the upper arm and abdominal wall. High echo around a breast cancer tumour is known as a halo; this high echo is observed in the lesion margin and indicates breast cancer cell infltration into the adipose tissue in the breast cancer margin. Te occurrence of a halo may be attributed to strong posterior scattering resulting from the difference in the speed of sound waves between cancer cells, which contain a large amount of water and adipocytes [18]. Using ultrasound images, Tohno and Bando observed weak echogenic areas in the breast cancer margin in the absence of cancer cell infltration into the surrounding adipose tissue [19]. Tese researchers also observed high echo in oedema-like functional changes caused by lymphostasis, which they referred to as a pseudohalo. In the two patients in our study, marked small vessels were observed in one patient and connective tissue proliferation in the other. We assume that posterior scattering occurred due to the proliferation of small vessels and connective tissue within the adipose tissue, which in turn, resulted in high echo in areas surrounding the tumours.
Terefore, we used ultrasonography to show that solitary glomus tumours are low-echo tumours with a diameter of up to 15 mm, exhibiting clear margins and a lack of lateral shadow. Blood fow inside the tumours was abundant, with frequent vessels fowing in and out of the tumours. Tus, glomus tumours should be considered in the diferential diagnosis of painful tumours ≤15 mm wherein blood-fow signals are observed.

Conclusion
Tis study constituted a retrospective analysis of ultrasonographic images containing solitary glomus tumours. Te results revealed that most tumours were low-echo tumours with a diameter of up to 15 mm, clear margins, and no lateral shadows. Abundant blood fow and vessels fowing in and out of the tumours were also observed. Moreover, the size of glomus tumours in areas other than the fngers was 5 mm or less; however, their depth/width ratio was greater than that of tumours of the fngers. Our study describes the ultrasonography characteristics of glomus tumours and reveals the importance of considering glomus tumours in the differential diagnosis of small painful subcutaneous tumours.

Data Availability
All data used to support the fndings of this study are included within the article.